Melatonin regulates oxidative stress and apoptosis in fetal hearts of pinealectomised RUPP rats

References

• Bae S, Xiao Y, Li G, et al. Effect of maternal chronic hypoxic exposure during gestation on apoptosis in fetal rat heart. Am J Physiol Heart Circ Physiol. 2003;285:H983–990.
   PubMed Web of Science ®Google Scholar
• Miranda JO, Ramalho C, Henriques-Coelho T, et al. Fetal programming as a predictor of adult health or disease: the need to reevaluate fetal heart function. Heart Fail Rev. 2017;22:861–877.
   PubMed Web of Science ®Google Scholar
• Rice MM, Landon M, Varner MW, et al. Pregnancy-associated hypertension and offspring cardiometabolic health. Obstet Gynecol. 2018;131:313–321.
   PubMed Web of Science ®Google Scholar
• Tripathi RR, Rifas-Shiman SL, Hawley N, et al. Hypertensive disorders of pregnancy and offspring cardiometabolic health at mid-childhood: project viva findings. J Am Heart Assoc. 2018;7. DOI:10.1161/jaha.117.007426.
   Web of Science ®Google Scholar
• Xue Q, Dasgupta C, Chen M, et al. Foetal hypoxia increases cardiac AT(2)R expression and subsequent vulnerability to adult ischaemic injury. Cardiovasc Res. 2011;89:300–308.
   PubMed Web of Science ®Google Scholar
• Gill C, Mestril R, Samali A. Losing heart: the role of apoptosis in heart disease – a novel therapeutic target? Faseb J. 2002;16:135–146.
   PubMed Web of Science ®Google Scholar
• Cornelius DC. Preeclampsia: from inflammation to immunoregulation. Clin Med Insights Blood Disord. 2018;11:1–6.
   Google Scholar
• Das UN. Cytokines, angiogenic, and antiangiogenic factors and bioactive lipids in preeclampsia. Nutrition. 2015;31:1083–1095.
   PubMed Web of Science ®Google Scholar
• Ditisheim AJ, Dibner C, Philippe J, et al. Biological rhythms and preeclampsia. Front Endocrinol Lausanne. 2013;4:1–8.
   PubMedGoogle Scholar
• Sedeek M, Gilbert JS, LaMarca BBM, et al. Role of reactive oxygen species in hypertension produced by reduced uterine perfusion in pregnant rats. Am J Hypertens. 2008;21:1152–1156.
   PubMed Web of Science ®Google Scholar
• Ovali MA, Uzun M. The effects of melatonin administration on KCNQ and KCNH2 gene expressions and QTc interval in pinealectomised rats. Cell Mol Biol (Noisy-le-grand). 2017;63:45–50.
   PubMed Web of Science ®Google Scholar
• Sun H, Gusdon AM, Qu S. Effects of melatonin on cardiovascular diseases: progress in the past year. Curr Opin Lipidol. 2016;27:408–413.
   PubMed Web of Science ®Google Scholar
• Gao L, Zhao YC, Liang Y, et al. The impaired myocardial ischemic tolerance in adult offspring of diabetic pregnancy is restored by maternal melatonin treatment. J Pineal Res. 2016;61:340–352.
   PubMed Web of Science ®Google Scholar
• Kim JH, Jeong SJ, Kim B, et al. Melatonin synergistically enhances cisplatin-induced apoptosis via the dephosphorylation of ERK/p90 ribosomal S6 kinase/heat shock protein 27 in SK-OV-3 cells. J Pineal Res. 2012;52:244–252.
   PubMed Web of Science ®Google Scholar
• Kudova J, Vasicek O, Ciz M, et al. Melatonin promotes cardiomyogenesis of embryonic stem cells via inhibition of HIF-1alpha stabilization. J Pineal Res. 2016;61:493–503.
   PubMed Web of Science ®Google Scholar
• Ozacmak VH, Barut F, Ozacmak HS, et al. Melatonin provides neuroprotection by reducing oxidative stress and HSP70 expression during chronic cerebral hypoperfusion in ovariectomized rats. J Pineal Res. 2009;47:156–163.
   PubMed Web of Science ®Google Scholar
• Uzun M, Gencer M, Turkon H, et al. Effects of melatonin on blood pressure, oxidative stress and placental expressions of TNFalpha, IL-6, VEGF and sFlt-1 in RUPP rat model of preeclampsia. Arch Med Res. 2017;48:592–598.
   PubMed Web of Science ®Google Scholar
• Nakamura Y, Tamura H, Kashida S, et al. Changes of serum melatonin level and its relationship to feto-placental unit during pregnancy. J Pineal Res. 2001;30:29–33.
   PubMed Web of Science ®Google Scholar
• Kivela A, Kauppila A, Leppaluoto J, et al. Serum and amniotic fluid melatonin during human labor. J Clin Endocrinol Metab. 1989;69:1065–1068.
   PubMed Web of Science ®Google Scholar
• Iwasaki S, Nakazawa K, Sakai J, et al. Melatonin as a local regulator of human placental function. J Pineal Res. 2005;39:261–265.
   PubMed Web of Science ®Google Scholar
• Okatani Y, Okamoto K, Hayashi K, et al. Maternal-fetal transfer of melatonin in pregnant women near term. J Pineal Res. 1998;25:129–134.
   PubMed Web of Science ®Google Scholar
• Lanoix D, Guerin P, Vaillancourt C. Placental melatonin production and melatonin receptor expression are altered in preeclampsia: new insights into the role of this hormone in pregnancy. J Pineal Res. 2012;53:417–425.
   PubMed Web of Science ®Google Scholar
• Hobson SR, Gurusinghe S, Lim R, et al. Melatonin improves endothelial function in vitro and prolongs pregnancy in women with early-onset preeclampsia. J Pineal Res. 2018;65(3):e12508.
   PubMed Web of Science ®Google Scholar
• Hobson SR, Lim R, Wallace EM. Phase I pilot clinical trial of antenatal maternally administered melatonin to decrease the level of oxidative stress in human pregnancies affected by preeclampsia. Methods Mol Biol. 2018;1710:335–345.
   PubMedGoogle Scholar
• Hobson SR, Lim R, Gardiner EE, et al. Phase I pilot clinical trial of antenatal maternally administered melatonin to decrease the level of oxidative stress in human pregnancies affected by pre-eclampsia (PAMPR): study protocol. BMJ Open. 2013;3:e003788.
   PubMed Web of Science ®Google Scholar
• Santiago-Font JA, Amaral LM, Faulkner J, et al. Serelaxin improves the pathophysiology of placental ischemia in the reduced uterine perfusion pressure rat model of preeclampsia. Am J Physiol Regul Integr Comp Physiol. 2016;311(6):R1158–R1163.
   PubMed Web of Science ®Google Scholar
• Li J, LaMarca B, Reckelhoff JF. A model of preeclampsia in rats: the reduced uterine perfusion pressure (RUPP) model. Am J Physiol Heart Circ Physiol. 2012;303(1):H1–8.
   PubMed Web of Science ®Google Scholar
• Schenone MH, Mari G, Schlabritz-Loutsevitch N, et al. Effects of selective reduced uterine perfusion pressure in pregnant rats. Placenta. 2015;36:1450–1454.
   PubMed Web of Science ®Google Scholar
• Kheradmand A, Alirezaei M, Asadian P, et al. Antioxidant enzyme activity and MDA level in the rat testis following chronic administration of ghrelin. Andrologia. 2009;41(6):335–340.
   PubMed Web of Science ®Google Scholar
• Güçlü O, Doğanlar O, Yüksel V, et al. FOLFIRI-mediated toxicity in human aortic smooth muscle cells and possible amelioration with curcumin and quercetin. Cardiovasc Toxicol. 2020;20(2):139–154.
   PubMed Web of Science ®Google Scholar
• Rocco L, Izzo A, Zito G, et al. Genotoxicity in zebrafish (Danio rerio) exposed to two pharmacological products from an impacted Italian river. J Environ Anal Toxicol. 2011;1(103):2161–2525.
   Google Scholar
• Glaab E, Garibaldi JM, Krasnogor N. Array mining: a modular web-application for microarray analysis combining ensemble and consensus methods with cross-study normalization. BMC Bioinformatics. 2009;10:358.
   PubMed Web of Science ®Google Scholar
• Alexander BT, Dasinger JH, Intapad S. Fetal programming and cardiovascular pathology. Compr Physiol. 2015;5:997–1025.
   PubMed Web of Science ®Google Scholar
• Simmons RA. Developmental origins of adult disease. Pediatr Clin North Am. 2009;56:449–466.
   PubMed Web of Science ®Google Scholar
• Asiltas B, Surmen-Gur E, Uncu G. Prediction of first-trimester preeclampsia: relevance of the oxidative stress marker MDA in a combination model with PP-13, PAPP-A and beta-HCG. Pathophysiology. 2018;25:131–135.
   PubMedGoogle Scholar
• Wang A, Liu Q, Zhang J, et al. Berberine alleviates preeclampsia possibly by regulating the expression of interleukin-2/interleukin-10 and Bcl-2/Bax. Int J Clin Exp Med. 2015;8:16301–16307.
   PubMed Web of Science ®Google Scholar
• Yawno T, Mahen M, Li J, et al. The beneficial effects of melatonin administration following hypoxia-ischemia in preterm fetal sheep. Front Cell Neurosci. 2017;11:296.
   PubMed Web of Science ®Google Scholar
• Miller SL, Yawno T, Alers NO, et al. Antenatal antioxidant treatment with melatonin to decrease newborn neurodevelopmental deficits and brain injury caused by fetal growth restriction. J Pineal Res. 2014;56(3):283–294.
   PubMed Web of Science ®Google Scholar
• Tain YL, Huang LT, Hsu CN. Developmental programming of adult disease: reprogramming by melatonin? Int J Mol Sci. 2017;18:426.
   PubMed Web of Science ®Google Scholar
• Chen YC, Sheen JM, Tiao MM, et al. Roles of melatonin in fetal programming in compromised pregnancies. Int J Mol Sci. 2013;14:5380–5401.
   PubMed Web of Science ®Google Scholar
• Savran M, Ascil H, Ozmen O, et al. Melatonin protects the heart and endothelium against high fructose corn syrup consumption–induced cardiovascular toxicity via SIRT-1 signaling. Hum Exp Toxicol. 2019;38:1212-1223.
   Web of Science ®Google Scholar
• Ali T, Mushtaq I, Maryam S, et al. Interplay of N acetyl cysteine and melatonin in regulating oxidative stress-induced cardiac hypertrophic factors and microRNAs. Arch Biochem Biophys. 2019;661:56–65.
   PubMed Web of Science ®Google Scholar
• Liu D, Ma Z, Di S, et al. AMPK/PGC1α activation by melatonin attenuates acute doxorubicin cardiotoxicity via alleviating mitochondrial oxidative damage and apoptosis. Free Radic Biol Med. 2018;129:59–72.
   PubMed Web of Science ®Google Scholar
• Ovey IS, Oncel CR. The effect of melatonin on digoxin induced cardiac damage in cardiomyocytes. Bratisl Lek Listy. 2019;120(1):78–85.
   PubMed Web of Science ®Google Scholar
• Reiter RJ, Mayo JC, Tan DX, et al. Melatonin as an antioxidant: under promises but over delivers. J Pineal Res. 2016;61:253–278.
   PubMed Web of Science ®Google Scholar
• Sottile ML, Nadin SB. Heat shock proteins and DNA repair mechanisms: an updated overview. Cell Stress Chaperones. 2017;23:303–315.
   PubMed Web of Science ®Google Scholar
• Doğanlar ZB, Uzun M, Ovali MA, et al. Melatonin attenuates caspase-dependent apoptosis in the thoracic aorta by regulating element balance and oxidative stress in pinealectomised rats. Appl Physiol Nutr Metab. 2019;44(2):153–163.
   PubMed Web of Science ®Google Scholar
• Abdulsid A, Hanretty K, Lyall F. Heat shock protein 70 expression is spatially distributed in human placenta and selectively upregulated during labor and preeclampsia. PloS One. 2013;8:e54540.
   PubMed Web of Science ®Google Scholar
• Abdulsid A, Lyall F. Heat shock protein 27 expression is spatially distributed in human placenta and selectively regulated during preeclampsia. J Reprod Immunol. 2014;101–102:89–95.
   PubMed Web of Science ®Google Scholar
• Fu N, Li H, Sun J, et al. Trichosanthes pericarpium aqueous extract enhances the mobilization of endothelial progenitor cells and up-regulates the expression of VEGF, eNOS, NO, and MMP-9 in acute myocardial ischemic rats. Front Physiol. 2017;8:1132.
   PubMed Web of Science ®Google Scholar
• Periasamy S, Mo FE, Chen SY, et al. Sesamol attenuates isoproterenol-induced acute myocardial infarction via inhibition of matrix metalloproteinase-2 and −9 expression in rats. Cell Physiol Biochem. 2011;27:273–280.
   PubMedGoogle Scholar
• Skau E, Henriksen E, Wagner P, et al. GDF-15 and TRAIL-R2 are powerful predictors of long-term mortality in patients with acute myocardial infarction. Eur J Prev Cardiol. 2017;24:1576–1583.
   PubMed Web of Science ®Google Scholar
• Jin Z, Zhang W, Yang H, et al. Maternal treatment with agonistic autoantibodies against type-1 angiotensin II receptor in late pregnancy increases apoptosis of myocardial cells and myocardial susceptibility to ischemia-reperfusion injury in offspring rats. PloS One. 2013;8:e80709.
   PubMed Web of Science ®Google Scholar
• Compernolle V, Brusselmans K, Franco D, et al. Cardia bifida, defective heart development and abnormal neural crest migration in embryos lacking hypoxia-inducible factor-1alpha. Cardiovasc Res. 2003;60:569–579.
   PubMed Web of Science ®Google Scholar
• Sugishita Y, Leifer DW, Agani F, et al. Hypoxia-responsive signaling regulates the apoptosis-dependent remodeling of the embryonic avian cardiac outflow tract. Dev Biol. 2004;273:285–296.
   PubMed Web of Science ®Google Scholar
• Hutter D, Kingdom J, Jaeggi E. Causes and mechanisms of intrauterine hypoxia and its impact on the fetal cardiovascular system: a review. Int J Pediatr. 2010;2010:401323.
   Google Scholar
• Patterson AJ, Zhang L. Hypoxia and fetal heart development. Curr Mol Med. 2010;10(7):653-666.
   Google Scholar
• Tuli HS, Kashyap D, Sharma AK, et al. Molecular aspects of melatonin (MLT)-mediated therapeutic effects. Life Sci. 2015;135:147–157.
   PubMed Web of Science ®Google Scholar
• Xu Y, Lu X, Hu Y, et al. Melatonin attenuated retinal neovascularization and neuroglial dysfunction by inhibition of HIF‐1α‐VEGF pathway in oxygen‐induced retinopathy mice. J Pineal Res. 2018;64(4):e12473.
   PubMed Web of Science ®Google Scholar
• Jin H, Wang Y, Zhou L, et al. Melatonin attenuates hypoxic pulmonary hypertension by inhibiting the inflammation and the proliferation of pulmonary arterial smooth muscle cells. J Pineal Res. 2014;57(4):442–450.
   PubMed Web of Science ®Google Scholar
• Spinale FG, Coker ML, Bond BR, et al. Myocardial matrix degradation and metalloproteinase activation in the failing heart: a potential therapeutic target. Cardiovasc Res. 2000;46:225–238.
   PubMed Web of Science ®Google Scholar